Thursday, May 29, 2014

One of the highlights of the Genomes to Biomes Conference was the 6th Symposium for Women Entering Ecology and Evolution Today (SWEEET-ness).

On a personal and professional level, I am all about encouraging anyone to pursue their dreams, to achieve their highest potential. I want to inspire others to be curious, to discover, and to encourage others to do the same. Perhaps it is because I am from Mexico, and grew up in the United States, that I am particularly keen on encouraging minorities in education and in science. Yet while women are not a minority in our society (in fact, human sex ratio allocation slightly favors women), they are a minority in science. In fact, while women are a majority in biological sciences at the undergraduate level, their representation in the field becomes a minority at the PhD level and continues to decline dramatically through increasing degrees of seniority in academia, from post-docs to associate and full professors. That's not right, and I hope to be a part of a cultural movement that changes things. For this reason, I attended to SWEEET symposium, as both a scientist, as a minority, and as a man.

It was not surprising to me that I, a man, was a minority as this symposium. To be honest, I was not sure if I should attend, not because I thought it would be awkward for me (anyone who knows me knows full well that I am not in the least discouraged by a room full of intelligent women), but because I did not want to affect the internal dynamic of a symposium for women in science, nor to take the place of a women interested in attending if there was limitations on the capacity of people that could register for this symposium. However, the moment I walked in the door, I was set at ease because of the women that I knew at that conference, both students and professors, friends and colleagues that I respect and admire.

The first part of the symposium was a talk given by a (male) researcher who studies why women are minorities in science, particularly in engineering, and why they are discouraged from careers in science. A major issue he addressed was the response to the "threat of stereotypes" where women who are in a work environment where they feel they are "dominated," consistently under-perform compared to control groups, groups of women that are not in a male "dominated" environment. This was tested by using male actors who were told to act "dominant' or "not dominant" when given an engineering problem they had to solve in collaboration with a woman test subject. After the exercise, these second year female engineering students were given a challenging test, which is actually the test to get a license in engineering. In this test, women who were in a "dominating" environment scored significantly less than women that were not in a dominating environment. An interesting point is that men also underperform in female dominated fields such as nursing. Thus, an important issue to first address is the intra-personal dynamics of "dominance" in the work environment, especially male dominated careers in academia.

In response to this talk, a critical point was brought up by McGill professor, Dr. Catherine Potvin (who also gave a lecture at the SWEEET) who said that part of the problem is how women interpret, or respond to, male behavior that they think is "dominating" or "sexist." This an important point, as the first lecture stressed how women that perceive being "dominated" in a sexist work environment underperform. Thus, she considers that part of the problem is that women often consider male behavior sexist, aggressive, or even harassing, when in fact, it is the meant to be the contrary, complimentary. She commented that she likes being complimented, and that women should not take compliments on their looks as something negative, but as something positive. She said that in her many years working as a scientist in Latin America, which is known to have a very sexist "macho" dominated society, she never felt that men were "dominating," nor did she ever feel belittled or harassed. In fact, she said that she had felt much more negatively about her interactions with males in academia in English-speaking universities than anywhere else. However, she also stressed that she has had wonderful allies in her career at McGill, men that have encouraged her to fight for professional equality and that have done even more than she said she could do for herself in promoting her and her excellence in science, for recognition of her achievements.

So what are potential solutions to this disparity in the demographic representation of women in science and inequalities in salary? One of the main points was that women need to "self-promote." Women need to be more confident that they are capable and qualified for positions that they apply for. This, in turn, would allow them to be more aggressive or assertive when they are in the process of negotiating for an academic position. This, would in turn, help to close the wage gap between men and women in science and other professional careers.

I also consider that a major issue that discourages women in science is the belief that for women need to act more like men to succeed in academia, or any other career where males are the majority. While I think that women need to be treated fairly and with respect on a personal and professional level, they should not be expected to think, or act like their male counterparts. Instead, they should be encouraged to think and act like women, especially in "male-dominated" careers because of what they can bring to the table, something new, a new perspective, a new way of doing things, an alternative to the way things are.

This may seem obvious, but in my own experience, I have met fellow graduate students in both the humanities and in natural science that are told by female advisors to act more like men, to be less feminine, to wear less makeup, to focus less on their looks, on wearing makeup and shopping, and focus more on their work. I have heard of advisors telling female students that they would be taken more seriously if they were less feminine. Thus, I think that the culture in academia needs to change. Men need to be more conscientious of how their behavior in the work-place can affect women, but women need to also realize that what makes then different to men should not be hidden or suppressed, but should be both celebrated and respected, both inside and outside of the academic environment.

"So what can men do?" I asked?

"Men can be powerful allies," said Dr. Alison Derry at the social mixer later that night. She stressed how grateful she is to have had great men in her life, from her father, to her husband, to her male colleagues that have encouraged her and supported her throughout her career. She also said she has had great men who have chaired the department and have been understanding of her and her responsibilities as a mother. This feeling was also shared by Dr. Potvin. Men that are not sexist, said Dr. Potvin at the symposium's question-and-answer panel discussion, need to take the place of sexist men, especially in positions where they can and do dominate the social environment and where they can actively discourage or suppress women in a professional environment.

My little sister, Julia, just graduated high school today and will be attending the University of California, Santa Cruz, to study biology. For Julia, and for all women in science, I wish you the very best, and I hope you know that you can count on me to be your ally. And if I pay you a compliment, please don't take it the wrong way. You rock!

Wednesday, May 28, 2014

I, like many
all graduate students, am primarily driven in life by the search for, and
attainment of, free food. Performing
experiments, writing your thesis, maintaining interpersonal relationships,
etc., are all important goals, but they pale in comparison to finding a
workshop that offers free pizza. This
primal drive is exhibited maybe most clearly at academic conferences, where
free food (and here I mean free as in “Buy this $2000 computer and get a free
mousepad”) is a predictable but limited resource.

The Genomes
to Biomes conference currently being held in Montreal is no exception. In fact, the different resource densities and
distribution patterns exhibited depending on the time of day (i.e. Welcome
Reception, morning coffee break, or poster session) provides the perfect
opportunity in which to study this behaviour.
There also happens to be some scientific talks going on at this
conference, which offer the chance to compare the behaviour of the graduate
student to the organisms they study, which range from daphnia to blue whales.

Starting
with the Welcome Reception at UQAM on Sunday night, small prey items, such as
scallop sliders, shrimp-kabobs, and tiny-steaks-in-a-spoon were moving freely
throughout the population. In some areas
of the habitat, like the far corners of the room, these prey items were found at
a fairly low density, which sometimes elicited a chase behaviour (very costly
in terms of social value) in order to secure a bite. However, I soon discovered that the space
right next to the catering door contained a very high density of prey, allowing
the students to simply stand in place, even continue their conversations (high
gains in social value), and the prey would actually APPROACH the students. This difference in behaviour depending on the
density of prey is mirrored in the blue whales that Jeremy Goldbogen studies (“Krill
density and depth distribution drive the optimal foraging strategies and
maneuverability of lunge feeding in blue whales”). He found (by tagging the whales with
accelerometers!) that when eating deep, dense patches of krill, whales tended
to swim in a fairly even plane, but when they encountered shallow, diffuse
patches of krill they became much more acrobatic, even performing 360° turns. The reason for this difference is likely due
to the energetic costs and pay-offs of the two strategies. However, please note that these results don’t
mean that you should perform somersaults at the Closing Reception in order to
get more dessert—it (probably) won’t work.

Moving to
the coffee breaks, where the food offered a high energetic value (you probably
don’t want to know how many calories are in one of those one-bite brownies) but
acquirement incurred an energetic cost in the form of queuing. However, the sharp (or desperate) ones among
you may have discovered that the queues on the top floor (Mont-Royal) were
considerably shorter than those on the Cartier/International floor. What compelled some people to disperse
downwards, while others dispersed upwards?
Sure, not wanting to walk up the stairs (thereby wasting valuable
brownie-calories) might be part of the reason, but perhaps those who went to
the top floor are genetically driven to explore strange new worlds, to seek out
new life and new civilizations, and to boldly go where no graduate student has
gone before. This was certainly what
Allan Edelsparre (“On the move: How food, genes, and environmental
heterogeneity affect dispersal”) found with his drosophila larvae—those with the
“rover” genotype had higher expression of a foraging gene that drove them to
travel longer and farther in their Petrie dishes in search of food than those
with the “sitter” genotype. These same
results were found in adult flies both in the lab and in the wild, where fluorescently-tagged
flies (sourced from a nearby drosophila all-night rave party) were released then
recaught at various distances from the release point. I propose someone (not me) take cheek swabs
from all attendees for genotyping at the foraging locus along with data on
which floor they foraged on.

Finally,
the last official food source of the day before the after-hours networking
drinking opportunities begin; the poster sessions. Any foraging behaviour at this event is more
difficult to ascertain due to confounding effects of alcohol availability, but I
will do my best. At this point in the
day, energy reserves are low and fatigue is high. Food is a highly sought-after resource, and
yet this is when prey distribution is at its most patchy—yesterday there were a
total of 4 bowls of pretzels per floor (trust me, I counted). This highly patchy distribution causes
students to aggregate around said bowls, making weak efforts to move towards
the closest poster, but often giving up halfway through their migration and
returning to the bowl. The parallels
between this behaviour and that of daphnia are uncanny. Audrey Reid (“Influence of prey patches on Daphnia pulex foraging behaviour”) found
that daphnia placed in tanks with patchy algae resources moved more slowly and
turned in more circles than those in tanks with evenly-distributed algae. She also found that growth was higher in the
patchy tanks, which is an effect I hope is not replicated in the student-pretzel
system (bathing suit season is just around the corner).

Unfortunately,
this blog post is going to press before the Closing Reception at the Sucrerie
de la Montagne on Thursday, so my observations on the behaviour of the student
in a highly novel environment (i.e. the napkin is not made of paper nor is the
cutlery made of plastic) will probably remain unpublished. I just hope I don’t end up lying on my back
in a pile of mud, in a futile effort to eat a piece of kelp (if you have no
idea what I’m talking about, find Katie MacGregor (“Crazy for kelp? Movement
behaviour of the green sea urchin (Strongylocentrotus
droebachiensis) in the presence of a preferred food”) and ask her).

*apologies
to the taxonomists in the crowd if this is not the correct binomial

Second day of the CSEE conference and
more exciting insides into eco-evolutionary research from all over
the world and all over the place. Our morning sessions covered mainly
ecological topics: One could learn how the distribution of plant
populations can be inferred by tracking pollen (Parker et al.: The
needle in the haystack: tracking pollen distributions to locate
important plant populations), and how population dynamics in small
rodents can be inferred by tracking regurgitates (Heisler et al.:
Picking up puke: A method to monitor small mammal communities across
landscapes) – quite a spectrum! Regarding anthropogenic impacts on
species and ecosystems, an interesting study from Lobo et al.
presented evidence for increased aggression and social dominance in
rodent populations from recently logged forest habitats. Vincent
Fugere presented a meta-analyses of selection coefficients imposed by
humans. Vincent found that, contrary to the expectation, selection
was reduced in many anthropogenic contexts, including habitat
disturbance and logging (Fugere and Hendry: Human influences on the
strength and shape of phenotypic selection). This is somewhat
paradoxical since many other studies found for e.g. strongly elevated
evolutionary rates in anthropogenic contexts (see e.g. Hendry and
Kinnison 1999 and follow up studies and meta-analyses).

On the other side of the hall, in the
“ecology and evolution” section, Rana El-Sawaabi (et al.)
presented her preliminary results from sticklebacks linking eco-evo
dynamics through the “elemental phenotype”: while phosphorous
concentration on stickleback’s body correlates with the degree to
which they express the armored phenotype, they find the surprising
result that more armored individuals are also the ones that excrete
more phosphorous to the environment. Their next goal is to determine
to what extent phosphorous availability constrains the development of
armor in freshwater (a trait that is often interpreted to respond to
predation pressure). This is interesting research in the context of
eutrophication and cascading ecosystem effects. Stay tuned!

Two afternoon highlights were the talks
by Em Standen (et al.) and Felipe Dargent (et al.) – both concerned
to look at evolutionary dynamics by manipulating environments of
focal organisms, in this case (of course) fish:

A while ago, Em decided to start
raising fish on land to see what happens.. sounds interesting? Yes,
it is. Standen et al. chose Polypterus as their model species
as this creature seems to be determined (well, at least
morphologically) to fill at least some of our gaps in knowledge about
the conquest of land by vertebrates. By raising Polypterus in
artificial lab environments that forced them to make a living outside
of the water, these fish explored an immense repertoire of behavioral
and anatomical plasticity, enabling them to move effectively on land
surfaces (well, at least for a fish that is). Very cool stuff!

Felipe, on the other hand, decided a
while ago to study guppies from different populations and
parasitation regimes in the context of what he calls “enemy
release”, i.e. under relaxed parasite pressure, to track down
changes in resistance evolution. Dargent et al. elegantly showed that
under relaxed selection (removal of the parasite in the wild) male
and female guppies rapidly evolve different trajectories of
resistance. While females, as they showed before, evolve increased
resistance after parasite removal, males increase their variance in
resistance but do not evolve increased (or decreased) resistance.
Since their replicated parasite-released populations were derived
from an ancestral population that was sexually dimorphic in
resistance (males more resistant than females) the evolution seen in
females but not males has led to an evolutionary loss of sexual
dimorphism – within 6-8 generations!

Tuesday, May 27, 2014

GENOMES TO/AUX BIOMES is off to a great start! Monday was the
first day of scientific presentations, with a huge range of interesting
presentations and posters. With parallel sessions on everything from the
ecology of mercury to Arctic and alpine genetics, there was something for
everyone. Two CSEE symposia and the CSEE
plenary talk were also held Monday, and were well attended. In the evening, a
public outreach lecture by Catherine Potvin, “Halting deforestation: One piece
of the climate mitigation puzzle” had Twitter abuzz (check out #G2B2014 to
follow along). Finally, things wrapped up for the day with a student and
post-doc mixer at a notorious Montreal bar, Saint-Sulpice. Conference
attendants packed the third floor, and visited tables in a speed dating-like
set up to talk about topics including job interviews, work-life balance, jobs
outside academia, and parenting as a grad student. Like any conference, it was
easy to get overwhelmed with all the interesting new science, but several
points stood out for me today, especially the morning CSEE symposium and the
CSEE plenary.

Last year, Ben and Kiyoko provided some great conference advice on this blog. One piece of advice was not to run around like a chicken
with its head cut off. There are so many interesting presentations and it’s
hard to make it to them all, so sometimes it’s best to pick an interesting
session and enjoy all the talks. The Centre Mont Royal has conference rooms
spread out over multiple floors, with many parallel sessions and a large symposium
every day.Today the auditorium played
host to two CSEE symposia: “Biodiversity change across spatial scales in the
Anthropocene” and “Effects of community diversity and composition on
evolutionary change”. It seemed like a great day to heed Ben and Kiyoko’s
advice, and take in the CSEE symposium talks. Although both symposia were
excellent, the morning session really got me thinking and excited about topics
I don’t usually spend a lot of time pondering.

The morning’s presentations featured a large range of study
systems: butterflies, bumblebees, and phytoplankton, oh my! I heard about
plants, corals, marine fishes, and meta-analyses that incorporated them all.
But overall, one question really stuck with me throughout the entire session:
are we (as scientists) asking the right questions? For many presenters, this
question was intertwined with the very important question of how to communicate
results about changes in biodiversity and biodiversity’s importance to the
public and policy makers. As Brian McGill pointed out, if we continually
communicate a message that species are declining, what are people to make of
species that are becoming very abundant, such as white tailed deer? Perhaps it
is better to speak or winners and losers of anthropogenic impacts. These
questions were highlighted for me by several interesting results presented
today. Mark Vellend talked about his work looking for biodiversity declines in
local-scale plant communities, but the perhaps surprising result was that he
observed no net changes. Next, Julia Baum presented results from marine
ecosystems. Using coarse scale biodiversity measures, the results seemed
similar: biodiversity was not declining, not until she teased apart harvested
and non-harvested species and saw declines in the latter. Of course for marine
systems, as Julia pointed out, there is also the problem of shifting baselines:
how can we measure biodiversity change when we have not even described a large
portion of marine biodiversity? This was also a challenge for Mary O’Connor’s
work on benthic marine communities. I was struck too by the data Jeremy Kerr
presented on bumblebees, indicating that they are losing ground at the southern
extent of their range while failing to expand their range northward.If the question we ask is about biodiversity
change, we may see the loss of bumblebees compensated by the gain of new
species, but will their role as pollinators be filled? Would we be asking the
right question? Graham Bell gave a very interesting talk that shifted the focus
just slightly. His work focusing on successive minima in phytoplankton abundance
allows him to investigate how the time to minima and the magnitude of minima
are indicative of underlying processes driving population dynamics. Finally,
Brian McGill’s talk really pulled the session together for me. He pointed out
that often measures of local biodiversity may appear constant despite species
turnover.The result may be homogenized
communities. What happens to ecosystem functioning when this occurs? What if we
lose bumblebees, or harvested fish species, but an invasive species increases
in abundance? Overall, the symposium really got me thinking and gave me a
different perspective on these issues.

Perhaps the highlight of the whole day for me was the CSEE
Plenary, given by Jeff Hutchings. Jeff gave an excellent talk that raised many
important questions about science communication and the role of science,
scientific advice, and peer review of scientific advice in policy decisions. In
illustrating these points, Jeff talked in detail about two topics that shaped
my interest in evolutionary ecology as an undergraduate student: Northern cod
and alternative mating strategies in Atlantic salmon. After the morning
session, where the question of how to communicate science effectively to policy
makers arose repeatedly, it was very interesting for me to consider these
familiar topics in terms of these important questions.

Growing up in Newfoundland, there is no escaping the story
of cod. If you ask much of my family, the word “fish” is interchangeable with
the word “cod”. Cod shaped the history of Newfoundland, but as Jeff explained,
their populations have declined by 97%. In some stocks, it’s as high as 99%. In
1992, the government announced a moratorium on cod, and predicted that the
stocks should recover to populations similar to those from the 1970’s within
two years. As most of us know, and Newfoundlanders know all too well, the
stocks did not recover in two years. Data that Jeff presented show that there
have been recent population increases, but once again the problem of shifting
baselines arises, as these levels are just a very tiny fraction of populations
observed in the first years of available data, themselves from the 1960’s after
hundreds of years of fishing. However, Jeff pointed out that based on these
increases, the cod quota has been increased. This disconnect between science
and policy highlights the need for science communication, good scientific
advice, and peer review of scientific advice.Late in 1992 I turned 4. I do not remember a time without a cod
moratorium in Newfoundland, and the story of the great fish that was no more
was one of those that lead me to study. It was one we often discussed during my
undergraduate classes at Memorial, and it was fun for me to think once again
about the story in the context of the earlier presentations.

A story that sparked my interest in evolutionary ecology was
the story of alternative mating strategies in Atlantic salmon. I audited a
class on alternative mating strategies taught by Ian Fleming at Memorial, and I
remember being fascinated by the examples we talked about in class. Jeff
explained his work looking at parr that mature very young in fresh water,
unlike older larger males that migrate to sea. Parr exhibit a rather unorthodox
sneak mating strategy during breeding events between larger males and females,
but they do contribute genetically to the offspring of these matings and the
parr strategy is heritable. Jeff pointed out that the absence of parr from the
recovery plan for Atlantic salmon demonstrates another example of a clear link
to policy, but where science could be better incorporated into policy. The
diversity of phenotypes that so vividly caught my attention in my undergrad are
important pieces of the diversity of Atlantic salmon populations, but were not fully
considered in policy decisions.

It was great to hear the sorts of questions I had been
thinking about all day applied to concepts I spent a lot of time considering as
an undergraduate. For me, it was a great way to wrap up a day of talks. Perhaps
you will find a similar opportunity at Genomes to Biomes, a chance to gain new
perspectives on familiar topics.

Monday, May 26, 2014

The excitement is in the air with the start of the GENOMES TO BIOMES Conference, which is the first-ever joint meeting of three of Canada's primier natural history societies, the Canadian Society of Ecology and Evolution, the Canadian Society of Zoology and the Society of Canadian Limnologists.At this meeting, 8 parallel sessions of talks spanning a large breadth of subjects, including ecology of biological invasions to evolutionary genetics. These talks will occur along with symposia of invited speakers. Today's (Monday) morning symposium is the CSEE Symposium on Biodiversity change across spatial scales during the anthropocene. In the afternoon will be the CSEE Symposium on effects of community diversity and composition on evolutionary change.Before commenting further on commentary of the conference itself, all of us in the Hendry Lab would like to get the shameless self promotion out of the way and encourage you to come to our presentations!!!

Monday, May 19, 2014

We all love to propose and debate “rules”, “laws”, and “conjectures” in ecology and evolution, although Andrew might have a particularlovefor this pastime. Such ideas help us to describe and understand the regularities we observe in the natural world – and the exceptions to them can reveal deeper levels of complexity and open up new avenues for research.

One rule that hasn’t been explored yet in this blog is Baker’s Rule (also called Baker’s Law). H. G. Baker observed, in 1955, that the flora of remote islands is typically composed of self-compatible species (much more so than continental flora), and explained this as a consequence of a negative interaction between self-incompatibility (SI, hereafter) and the process of colonization. A self-compatible species can found a new population through the dispersal of a single seed. However, SI species have a harder time of it for several reasons:

A single seed from an SI species would produce a plant incapable of becoming fertilized;

Two, three, or even more seeds might together contain insufficient allelic diversity at the SI locus to allow cross-fertilization and population growth, depending on the allelic diversity of the source population and the luck of the “founder effect” draw from it;

Worse still, even if sufficient allelic diversity is present at the outset, SI alleles might be lost due to drift while the founding population is still small, and such reductions in allelic diversity might render the population inviable.

According to Baker’s Rule, then, SI species require the concerted dispersal of multiple seeds to colonize new sites. This might not be difficult for nearby sites, but for long-distance colonizations it apparently presents a substantial hurdle that leads to the observed under-representation of SI species at sites such as remote islands. Baker’s Rule has been investigated extensively since it was proposed, and it seems to be broadly true, although there are a number of exceptions to it as well.

Mike Nowak, myself, and Anne Yoder recently had a paper published in JEB about an exception that is of particular interest because it concerns Coffea, the beloved genus that provides us with the coffee bean. Julia Child once quipped that “it is difficult to imagine a civilization without onions”, but I would submit that it is even more difficult to imagine modern civilization without coffee. More scientifically, the exception we studied is of particular interest because of the very long distance over which dispersal and colonization was achieved: from Madagascar or even mainland Africa (which one is not known), all the way to the remote Pacific island of Mauritius. The several Coffea species involved here are apparently self-incompatible, which makes this very long-distance colonization a notable exception to Baker’s Rule.

Let’s review the geography a bit:

On the left is the southeastern coast of Africa, with Madagascar, the fourth-largest island in the world, to its right. Over on the right-hand edge is Mauritius, about 2000 km from the African mainland and more than 1000 km from the east coast of Madagascar. Mauritius is a volcanic island that formed about 8 million years ago, and is best known as the home of the now-extinct dodo (itself an interesting case study in long-distance dispersal and colonization). Africa, Madagascar, and Mauritius all have their own Coffea species, and the little phylogenetic tree at the upper right shows their relationships, which remain poorly resolved. (There is also Coffea on La Réunion, the other member of the Mascarene Island group shown here, but that Coffea almost certainly arrived later, from Mauritius, so I won’t discuss it here.) Mauritius is a very small island, just over 2000 km2 in size, so it presents an inviting but difficult-to-hit target for seeds from Madagascar or the mainland:

Mike has been doing a lot of hard work in this system for some years now. Mike provided me with a photo from his time there; let us all take a moment to pity the life of the tropical field biologist.

These sorts of pursuits keep Mike very busy (plus, less tongue-in-cheek, he has just started a new job at the University of Oslo; I imagine he’ll be working hard to get funding to go back to Mauritius next winter!), which is why I’m writing up our paper for the blog. That means I’m going to skim over a good deal of the amazing work that Mike has done in the system:

He obtained new evidence establishing the self-incompatibility of Mascarene Coffea, based on controlled self-pollinations of bagged flowers in wild populations:

He provides a new, and likely much more accurate, estimate for the date of Coffea’s colonization of Mauritius: probably between 1.80 and 2.64 million years ago. Notice how long it took for successful colonization to occur, after the formation of the island ~8 million years ago – overcoming Baker’s Rule is not trivial. On the other hand, a couple of million years is not such a long time on evolutionary timescales.

Mike also produced a gene tree for the SI allele (S-RNase) diversity in African, Malagasy, and Mascarene Coffea; I'll discuss the significance of it below. Click to see it larger, or better yet, look at it in our paper, Fig. 3:

These results lay the foundation for what I’m going to talk about for the rest of this post: estimating the size of the founding population. Mike’s results above establish that the colonization of Mauritius occurred too long ago for neutral genetic markers to be useful in estimating the founding population size. However, because these Coffea species are self-incompatible, their SI alleles are subject to negative frequency-dependent selection (NFDS): rare SI alleles are favored because plants possessing them can cross widely, whereas very common SI alleles are disfavored because the crossing of plants possessing them is hindered. These dynamics mean that SI alleles (like alleles at other loci subject to NFDS, such as MHC alleles) tend to be preserved over very long periods of time – indeed, so long that essentially the same SI alleles are observed in various Coffea species that diverged millions of years ago. This leads to a pattern called trans-specific polymorphism: polymorphism at a locus that is sustained even across speciation events. The gene tree Mike obtained, shown above, displays a clear pattern of trans-specific polymorphism: SI alleles drawn from across African, Malagasy, and Mascarene species are often more closely related to each other (because they share the same ancestral allele) than are SI alleles drawn from just one of those groups. A more visual way of saying this is that the red, blue and green colors (representing alleles from the African, Malagasy, and Mascarene groups) are sprinkled across the gene tree, and often co-occur within a single subclade – very different from the more typical pattern of intraspecific polymorphism that would lead to one cluster of red alleles, one cluster of blue alleles, and one cluster of green alleles in the gene tree. Once you wrap your brain around this fact, it is very cool, because it means that as far as the SI alleles are concerned, the colonization of Mauritius might as well have happened quite recently; 100 years ago, say. Apart from the possible early loss of SI alleles due to drift when the founding population was still very small, the SI allelic diversity in Mauritius today is likely the same as it was at the time of colonization. It can therefore be used to determine the size of the founding population.

How? Well, suppose you know the number of distinct SI allelic lineages in the source population; a likely estimate for this system is 30 (see the paper for supporting citations). Now pick a founding population size; 10 seeds, let’s say. The SI allelic diversity at the moment of founding is easy to calculate, based simply on sampling the source population. Now you just need to run time forward a bit, with reasonable estimates of the population growth rate and such, to allow drift to cause the loss of some alleles early on. Once the population reaches a sufficient size (we used N=5000, which is extremely conservative), SI alleles will essentially never be lost due to drift, even over millions of years, because of the NFDS acting on them. Once your simulation reaches that point, then, you have one estimate of how much SI allelic diversity would be expected today, based on a colonization event millions of years ago involving the parameter values you chose (here, 10 seeds from a source population with 30 distinct SI alleles). You can run this stochastic simulation many times with the same parameters, to get a full distribution of the expected number of SI alleles – and then you can vary the parameters, to see how that distribution changes. Inspired by a similar study in Darwin’s finches (Vincek et al. 1997), that’s what I did, in my contribution to the paper:

This is our key result (again, click to see it larger). Panel A shows the distribution obtained for 30 SI alleles in the source population, given a number of founders (Nf) ranging from 1 to 50. Now the question becomes very simple: what values of Nf produce a distribution that overlaps well with the observed number of SI alleles in Mauritian Coffea today (seven)? If you start with three or fewer founders, you never get seven or more SI alleles at the end, because it is mathematically impossible for the founders to carry that many different alleles. If you start with ten or fewer founders, it is somewhat unlikely that you will end up with as many as seven SI alleles, although it does happen sometimes. If you start with more than 25 or so founders, on the other hand, it is unlikely that you will end up with as few as seven SI alleles. There is a “sweet spot” of about 11–24 founders that is most likely to result in the allelic diversity observed today; with 15 founders, seven SI alleles at the end is the median result, and so perhaps it is a “best estimate” of the founding population size.

How much does this conclusion depend upon the allelic diversity of the source population, As? Not very much, as it turns out. Panel B shows a summary of the same results for different values of As from 10 to 34 (34 being about the maximum plausible value); now only the mean (not the median) of the distribution is shown, for simplicity. It can be seen that the results for different values of As are quite similar until the number of founders gets quite large; regardless of As, then, the founding population looks likely to have been roughly 11–24 individuals in size.

Now, this is somewhat of an oversimplification. Results are somewhat sensitive to the rate of population growth (slower growth leads to more generations in which drift plays a substantial role in the process), and Coffea disperses in fruits that actually contain two seeds (coffee “beans”) which complicates things somewhat, and so forth (see the paper for details). But the upshot is clear: at least five seeds (and thus three fruits) were likely required for colonization to succeed and produce the present-day population, whereas it is very unlikely that more than 31 seeds were involved. The fact that a synchronous dispersal of several-to-many seeds apparently managed to arrive at Mauritius over more than 1000 km of open ocean and establish a new population there is quite remarkable, and demonstrates that Baker’s Rule, while a useful rule of thumb, is far from ironclad. Furthermore, the fact that it took only a few million years from the formation of Mauritius to its colonization by Coffea, despite Baker’s Rule, suggests that such long-distance dispersal events might not be as unlikely as is commonly assumed.

Friday, May 16, 2014

My last post used the Mallard as an example of a species
that seems to fit in everywhere without difficulty. I used this ultimate
generalist to discuss the theory of ecological fitting. The present post is
about another duck that is quite different: the Wood Duck, which I will use to
discuss the “Law of the Unspecialized.”

While no one seeks out pictures of Mallards, everyone seeks
out pictures of Wood Ducks – they are spectacular birds. In fact, for me, they have
always been one of those trophy birds that I would get super-excited about seeing
– something to write home about and for which to hide for hours in the bushes hoping
that one would come near. My kids love Wood Ducks too, partly because we occasionally
see a few while kayaking near our house and partly because of the Duck's Unlimited book “A House for Wanda
Wood Duck.”

In the book, a (human) family has a Wood Duck that
nests each year in a hollow tree beside their pond, but one day the tree blows
down. The kids are devastated, but Dad saves the day by building a Wood Duck
box. The box is mounted on a stump, the duck appears, the babies hatch, the
kids are excited, and everyone is happy – including my kids. I had read this
book to my kids many times and each time I had noted to them the instructions on
the last page for building a Wood Duck box. Each time, I would tell the kids: “One
day I will build a box and we will see if Wanda will ditch that clingy family
in the book and come to our house” – but, year after year, I put the book away
and never got around to building the box. Then, one rainy spring day a couple
of years ago, I finished reading the book and decided: “Damnit, I am going to
do this RIGHT NOW.” So the kids and I built the box according to the
instructions in the back of the book and mounted it on a tree over the canal on
which we live. “Well, that was fun, kids - but don't expect too much.”

A male Wood Duck outside our house.

The next morning I was awakened by my wife, Heather, telling me
to look outside. There, sitting on a branch looking greedily up at our new box,
was a female Wood Duck. Rarely have I received such unexpectedly instant gratification.
That first year and the subsequent year, we “raised” a family of Wood Ducks in
the box. We rarely saw the adults, and we never saw the babies, but we know it
worked because we would occasionally see the female going in or out and – at the
end of the summer – I opened the box to see the egg shells. Knowing that we
were successful but so rarely seeing the birds made us wish each year for a peep-hole
into the box, something we could open up to look in at the female and her eggs.
So, this year, we finally built a little door in the side of box, mounted the
box even before the ice was out, and were again gratified by soon seeing a Wood
Duck coming and going.

A Wood Duck checking out the view from our box.

A few days ago, I finally put the peep-hole to the test. I
put a ladder against the tree, undid the clip for the small door we had added,
and slowly opened it up. There she was, sitting in the bottom of the box. She
even let me stick my camera into the box to take pictures. It was remarkable –
almost like she was comatose or pretending to hide. “You can’t see me. You can’t
see me. You can’t see me.” (I am reminded of those movie scenes where a cop
knocks on a door of an apartment and the clueless bad guy inside yells “No one’s
here!”) Eventually, I guess I was too invasive and she fled, revealing 15 eggs.
I worried that I might have permanently frightened her away, but she was soon
back. It was crazy really: a huge scary creature climbs your tree, tears apart your nesting site, sticks big objects that flash inside, and you flee in abject
terror. Moreover, our cat – despite our efforts to discourage him – keeps sitting
on top of the box presumably hoping to snag some Canard Confit on the way in or
out. Yet she keeps coming back. Does she have nowhere better to go?

You can't see me. You can't see me. I'm not here.

So, this got me to thinking. If a Wood Duck shows up at a
brand new box within an hour of putting it up, and keeps coming back despite
discovering its permeability to scary mammals, nesting sites must be extremely
limited. Indeed, the Wood Duck is an obligate tree cavity nester, such that the
number of nesting pairs will inevitably be limited by the number of available cavities.
This presumably means that a bird that gives up on a less-than-optimal cavity
might not find another one. Indeed, the push in the 1930s to put up Wood Duck
nest boxes apparently dramatically increased Wood Duck numbers to the point
that they are considered of “Least Concern” by IUCN.

Of "Least Concern"

But why should Wood Ducks be so specialized in their choice
of nest sites? Why not nest on the ground? Mallards do it and are doing very
well – certainly much better than Wood Ducks. Certainly tree cavities and nest
boxes give at least some protection against (real) predators, and so I can see
a good reason to start nesting there – and to then adapt to those conditions.
For instance, Wood Ducks are remarkably adept at getting in and out of small
holes on vertical trees and their young can leap out of the hole and fall 60
feet without injury, like fluffy little ping pong balls. Yet, what does a duck
do when it can’t get a nesting hole? Does it just not breed at all? Does it try
to nest on the ground? Either way, specializing on tree holes seems a great way
of evolutionarily painting yourself into a corner.

Little do they know they are trapped to repeat the nest box scramble.

Here, then, we have a clear case of a species specializing
so strongly on a particular resource (tree cavities) that it ultimately traps
itself in a situation where it will forever be marginal. And this
specialization is particularly problematic should conditions change, such as
when logging, agriculture, and urbanization dramatically reduced tree cover in
North America. Of course, this result partly shows that evolution is not
forward-looking and does not work for “the good of the species.” Instead, evolution
tinkers with what is present and selects on the basis of what is good for an
individual. That is, the individuals that first used tree cavities – and that
were better adapted for those cavities – had higher fitness and so the use of
tree cavities and specialization on them increased through time even though it
would eventually cause species-level problems, especially when the environment changes unfavorably (loss of trees). (Here I am reminded of “evolutionary traps” or – in extreme cases – “evolutionary suicide”, although better examples certainly exist.)

I was pondering these ideas today right around the time that
I need to take my morning constitutional to the reading room. Of course, one
needs something to read in the reading room and so I picked up the journal that
happened to be lying around: the October 2013 issue of Evolutionary Ecology
Research. (How I miss the days of routinely browsing printed journals.) Sitting
down and opening up the issue, I saw the first article: “Cope’s Law of the Unspecialized …” by Pasquale and Fortelius. Hmmm, I knew of Cope’s Rule
(organisms tend to get larger through evolutionary time) but not Cope’s Law.
Having an academic interest in Laws-Rules-Conjectures and the like, I read on. “… new major taxa are more likely to originate from a
generalized, rather than a specialized, member of the ancestral taxon …” (Pasquale
and Fortelius 2013, p. 748). Right then and there, I felt a blog coming on. I had heard of this sort of logic before, although not under
that name. That is, new adaptive radiations tend to be founded by generalist species
and new species in the radiation then increasingly specialize in ways that lead
them toward evolutionary dead ends. Most derived species simply become so
specialized for a particular mode of existence that they are unlikely to explore
new strategies. Stated another way, specialist-derived species get stuck
on an adaptive peak surrounded by a low-fitness moat. As a result, they simply
can’t evolve away from their local peak – even though other nearby fitness peaks
might be much higher. Although evidence for this idea of dead-end specialists is
mixed, I think the Wood Duck provides, if not proof, at least a potential
iconic example: the generalist Mallard is much more likely to persist and to
generate the next radiation of ducks than is the Wood Duck. Of course, other
examples are even more obvious. Specialist parasite lineages are unlikely to
outlive their host lineages, and some “hyperparasites” specialize on parasites
that specialize on parasites that specialize on parasites. Alpine specialist
plants on mountaintops surrounded by warm climates (sky islands) will go
extinct with climate change. Nevertheless, the Wood Duck Rule sounds better
than the Mallard Rule or the Hyperparasite Rule or the Sky Island Rule. I suppose
the Koala Rule or the Giant Panda Rule might have the same cachet though.

Presumably the way to break the Wood Duck Rule would be to
have your adaptive peak simply disappear, leaving you no choice but to evolve
toward a new peak. Of course, you would also have to have high enough fitness in
the new environment to attain positive population growth, and you would have to
be protected against homogenizing gene flow from the initially more-abundant
specialist members of your species (the ephemeral divergence hypothesis again).
So we need to conduct an experiment. We need to take a specialist away from its
original environment and place it into a new environment where it must then
embark on a new evolutionary trajectory – and we can remove the above
constraints by (initially at least) creating otherwise benign conditions (no
predators, supplemental food) and by preventing gene flow from the ancestral
group.

Potential gene flow.

So, when I get home tonight, I am going to capture some Wood
Duck adults and place them into a large cage in my yard so they can’t leave
and so predators – including my cat – can’t get at them or their eggs. The cage
will extend into the canal so they can still get food. I will also take down
the nest box, cut down the tree, and place some nice, Mallard-style nesting areas
(the new habitat) in strategic locations. Then I will kayak around the entire
area and shoot all cavity-nesting Wood Ducks (I suppose that will have to be
all other Wood Ducks) or, perhaps better yet, simply knock down all nest boxes
and block all tree cavities. Then I – and maybe my kids – will continue this experiment
for the next 50 years or so and see what we get. Today’s Wood Ducks might hate
it but tomorrow’s Wood Ducks will thank us. Just kidding.

Monday, May 5, 2014

One of the core processes underlying evolution is natural selection. Natural election is a process by which organisms adapt to their environments, and is why we have the phenotypic variation (a.k.a. biodiversity) we observe today. These days, we have literally thousands of estimates of selection for all sorts of organisms, and there are now several meta-analyses in the literature examining patterns of phenotypic selection. One of the patterns considered is temporal variation in selection; some analyses argue that there is considerable temporal variation in selection, whereas others argue there is very little. So which is it, and more importantly, how important is this temporal variation in our understanding of adaptation and evolution?One more thing to consider with temporal variation in selection is how
important is this variation in comparison to other patterns of
selection, with one obvious consideration being spatial variation.

Typically, when considering patterns of selection, we estimate selection by considering a trait under selection and a fitness measure. However, there are logistical problems with this. For example, what’s the best way to measure fitness? Survival? Sure, but if you don’t reproduce, is survival then a good estimate of fitness? Fecundity? Great, but what if none of your offspring make it to maturity – is fecundity then a good estimate of fitness? As you can see, quantifying fitness can be difficult, especially in nature.

An organism in nature. Is it fit or not?
Photo: Kiyoko Gotanda

So what’s an evolutionary biologist to do? How about considering the consequences of selection? If selection is ‘doing its job,’ then we should see changes in the trait under selection, right? If there is selection for larger body size within a population, then we would expect that population to evolve toward an increased mean body size. So, instead of trying to estimate selection, what if we looked at the phenotypic trait that is purportedly under selection? This might be handy because (1) quantifying a phenotypic trait through time is easier than trying to accurately estimate fitness in natural populations, (2) we can consider the importance of temporal variation in selection, because if selection is acting on a trait, and that selection is varying, then it’s reasonable to think that the trait would also vary through time, and (3) compare temporal variation to spatial variation to get a sense of the relative importance of variation in time and space. Thus, we decided to go out and measure spatiotemporal variation in an adaptive phenotypic trait.

First, we needed a system where we have some a priori knowledge about selection and adaptive traits. If we wandered into a random system and quantify a phenotypic trait, we would have no idea if that particular trait was an adaptive trait, nor if and where selection was acting, etc. We’re pretty lucky that there are now several systems we can choose from in which we know that adaptive traits are under selection; the system we chose is male colouration in the Trinidadian guppy system. For those unfamiliar with the guppy system, I refer you to our previous posts here, here, here, and here.

Lovely Trinidadian rainforests
Photo: Kiyoko Gotanda

So we trudged through the gorgeous rainforests of northern Trinidad, caught guppies, and photographed them. We sampled ~20 male guppies annually for six years at six different sites within two rivers. Within the Marianne River, we selected two high-predation (HP) sites and two low-predation (LP) sites, and within the Paria River, we selected two sites, both LP. Male guppies were photographed, and then I (with the help of several audiobooks) quantified their colour patterns from the digital photographs.

Colourful guppies

So what did we find? Not surprisingly, LP sites had more colour than HP sites. I know, you can stifle your yawns: no surprise there. Are you surprised? Here's some background information on why it's not a surprise. Two things about this were interesting, though. First, everyone assumed guppy colour was relatively temporally stable since the
HP/LP colour divergence has been demonstrated many times. However, nobody
has actually assessed colour annually for several years! If you take a quick peak below, there was some temporal variation, but the LP sites, with two exceptions, basically had more colour than HP sites for six years. The second thing to consider is that there are many potential sources of temporal variation in male guppy colour such as seasonal flooding, variation in parasite loads, and variation in predator composition and density. We don't see any evidence of that here, but this might be due to sampling at the annual level. If we sampled several times a year, we might find a different story. This is a perfect excuse for more trips to Trinidad!

Second, one of the LP sites achieved high colour differently than other sites, and that pattern is relatively consistent through time. Take a look above. The solid, black lines are LP sites, and the dashed lines are HP sites. So, above, you see most of the solid lines above the dashed lines, meaning all the LP sites generally have more colour (carotenoid, structural and melanins) than the HP sites. Now take a look below at graph only showing carotenoid (orange and yellows) colours. You can see one set of the solid, black lines hanging out with two dashed lines.you've for an LP site hanging out with the HP sites in terms of carotenoid colours. In other words, one of these LP sites (which happens to be called M16) and HP fish do not have a lot of orange colouration compared to the three other LP sites.

Now check out the structural (violet, silver, and blue) colour graph below. Again, one of the solid black lines seems to be hanging with the dashed line. That solid line happens to be M16 (legend in first graph above) again! So one LP site (M16) and HP fish have more structural colouration than three other LP sites. So this one LP site (M16) has lots of colour, but unlike the other LP sites, achieved more total colour with more structural colouration and less carotenoid colouration. This pattern holds over six years, so it seems like whatever is happening at M16 isn’t going to be changing anytime soon…

So, what can the spatiotemporal patterns of male guppy colour tell us about selection? We can infer that spatial variation in selection is more important than temporal variation in selection on male guppy colour in our sites over our time frame. Now, before you bombard us with comments about how can we possibly make statements about selection when we didn’t measure selection, let us offer a few of our own comments. First, we recognize that the guppy system might be exceptional in terms of spatial variation in selection vs. temporal variation in selection. The guppy system is known for strong spatial variation in selection on adaptive traits, which is a reason why many researchers gravitate towards guppies for their research. Second, quantification of an adaptive trait is looking at the consequences of variation in selection. That being said, we are confident that we can interpret our results in the context of selection (without having directly estimated selection) because previous work has shown many known selective factors appear to vary more spatially than temporally (e.g. predation regime, canopy cover, and parasitism). Third, we are not suggesting that our approach should replace the direct estimation of selection, but instead, that it should be used to provide important information that is complementary to our understanding of selection in natural populations.